Assessing the durability and efficiency of landscape-based strategies to deploy plant resistance to pathogens

Rimbaud, Loup; Papaïx, Julien; Rey, Jean‐François; Barrett, Luke G.; Thrall, Peter H.

doi:10.1101/260836

Cited by 10 publications

(17 citation statements)

References 185 publications

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“…Transmission between fields can be predicted from spore dispersal (Marcroft et al, 2004;Bousset et al, 2015). Thus, spatially explicit models can be used to study and ultimately design combinations of landscapes, varietal choice and tillage practices promoting resistance durability against phoma stem canker (Lô-Pelzer et al, 2010;Rimbaud et al 2018). As to the practicalities of spatial organization of the landscape, lessons have to be learned from the available case studies.…”

Section: Discussionmentioning

confidence: 99%

Careful deployment of oilseed rape crops with Rlm6 resistance gene against L. maculans is recommended to prevent the loss of efficacy of this resistance gene in French condiment mustard

Bousset

Ermel

Delourme

2018

Preprint

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1 Careful deployment of oilseed rape crops with Rlm6 resistance gene against L. maculans is recommended to prevent the loss of efficacy of this resistance gene in French condiment mustard. AbstractBreeding varieties for increased disease resistance is a major means to control epidemics. However, the deployment of resistance genes through space and time drives the genetic composition of the pathogen population, with predictable changes in pathotype frequencies. In France, Leptosphaeria maculans causes disease on Brassica napus oilseed rape crops but not on B. juncea condiment mustard. Prior to the deployment of winter B. napus varieties with Rlm6 resistance gene introduced from B. juncea, the aim of our study was to investigate if this deployment could impact disease control in condiment mustard. We assessed the presence of resistance genes against phoma stem canker in a set of current French B. juncea varieties and breeding lines. Rlm6 was detected in all the 12 condiment mustard varieties. Rlm5 was also detected in 8 varieties. No additional resistance genes were detected with the set of isolates used. Because frequency of isolates virulent on Rlm6 is very low, these results indicate that Rlm6 gene is a major component of disease control in the French B. juncea mustards tested. Using Rlm6 in oilseed rape varieties will very likely induce an increase in frequency of Rlm6 virulent isolates. This raises the acute concern of a wise deployment of oilseed rape around the condiment mustard growing area. Scientific knowledge on adaptation dynamics, spatial segregation of crops and cooperation between actors is currently available in order to mitigate the risk and advert negative consequences of the introduction of Rlm6 resistance gene in oilseed rape varieties.

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Section: Discussionmentioning

confidence: 99%

Careful deployment of oilseed rape crops with Rlm6 resistance gene against L. maculans is recommended to prevent the loss of efficacy of this resistance gene in French condiment mustard

Bousset

Ermel

Delourme

2018

Preprint

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“…The model used in this study is an adapted version of that presented by Rimbaud et al (2018b), which simulates the clonal reproduction, spread and evolution of a pathogen in an agricultural landscape over multiple cropping seasons. Here, we introduce between-season sexual reproduction to address the issue of pathogens with mixed reproduction systems.…”

Section: Model Overviewmentioning

confidence: 99%

“…Here, we investigated the effect of pathogen sexual reproduction on the evolutionary and epidemiological control achieved with four main categories of deployment strategies (rotation, pyramiding, mixture and mosaic). We adapted the landsepi model (Rimbaud et al, 2018b), which simulates the spread of epidemics across an agricultural landscape and the evolution of a pathogen in response to the deployment of host resistance, to include pathogen sexual reproduction. We then used this model to compare the resistance deployment strategies considered for situations in which two major resistance genes conferring immunity are deployed.…”

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confidence: 99%

Effects of pathogen sexual reproduction on the evolutionary and epidemiological control provided by deployment strategies for two major resistance genes in agricultural landscapes

Zaffaroni

Rimbaud

Rey

et al. 2023

Preprint

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Resistant cultivars are of value for protecting crops from disease, but can be rapidly overcome by pathogens. Several strategies have been proposed to delay pathogen adaptation (evolutionary control), while maintaining effective protection (epidemiological control). Resistance genes can be i) combined in the same cultivar (pyramiding), ii) deployed in different cultivars sown in the same field (mixtures) or in different fields (mosaics), or iii) alternated over time (rotations). The outcomes of these strategies have been investigated principally in pathogens displaying pure clonal reproduction, but sexual reproduction may promote the emergence of superpathogens adapted to all the resistance genes deployed. We improved the spatially explicit stochastic modellandsepito include pathogen sexual reproduction, and then investigate the effect of sexual reproduction on evolutionary and epidemiological outcomes across deployment strategies for two major resistance genes. Sexual reproduction only favours the establishment of a superpathogen when single mutant pathogens are present together at a sufficiently high frequency, as in mosaic and mixture strategies. We concluded that, although sexual reproduction may promote the establishment of a superpathogen, it did not affect the optimal strategy recommendations for a wide range of mutation probabilities, associated fitness costs, and landscape organisations (notably the cropping ratio of resistant fields).

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“…Related approaches such as geographic mosaics should likewise decrease connectivity between susceptible hosts and so have analogous effects at broader spatial scales (Finckh & Wolfe, 2006; Knott, 1972). The ratio and aggregation of different resistant types can be further modified to influence connectivity and encounter rates at landscape scales (Papaïx, Touzeau, Monod, & Lannou, 2014; Rimbaud, Papaïx, Rey, Barrett, & Thrall, in press). Similarly, it is common practice to temporally rotate different varieties or crop types among fields to interrupt disease transmission cycles (Bousset & Chèvre, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…However, empirical studies are needed to validate theoretical predictions regarding how best to manipulate the diversity of resistance in landscapes to alter transmission and pathotype composition of populations. Experiments able to simulate contrasting distances among populations, cross‐year survival, and varying levels of inoculum admixtures from sub‐populations comprised of different plant genotypes would be of great value for testing resistance gene deployment strategies identified by models (Lô‐Pelzer et al., 2010; Hossard, Jeuffroy, Pelzer, Pinochet, & Souchère, 2013; Hossard, Gosme, Souchere, & Jeuffroy, 2015; Rimbaud et al., in press). One challenge associated with experimental approaches is to effectively identify effects at field scale that may actually occur at large scales.…”

Section: Introductionmentioning

confidence: 99%

Spatio‐temporal connectivity and host resistance influence evolutionary and epidemiological dynamics of the canola pathogen Leptosphaeria maculans

Bousset

Sprague

Thrall

et al. 2018

Evolutionary Applications

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Genetic, physiological and physical homogenization of agricultural landscapes creates ideal environments for plant pathogens to proliferate and rapidly evolve. Thus, a critical challenge in plant pathology and epidemiology is to design durable and effective strategies to protect cropping systems from damage caused by pathogens. Theoretical studies suggest that spatio‐temporal variation in the diversity and distribution of resistant hosts across agricultural landscapes may have strong effects on the epidemiology and evolutionary potential of crop pathogens. However, we lack empirical tests of spatio‐temporal deployment of host resistance to pathogens can be best used to manage disease epidemics and disrupt pathogen evolutionary dynamics in real‐world systems. In a field experiment, we simulated how differences in Brassica napus resistance deployment strategies and landscape connectivity influence epidemic severity and Leptosphaeria maculans pathogen population composition. Host plant resistance, spatio‐temporal connectivity [stubble loads], and genetic connectivity of the inoculum source [composition of canola stubble mixtures] jointly impacted epidemiology (disease severity) and pathogen evolution (population composition). Changes in population composition were consistent with directional selection for the ability to infect the host (infectivity), leading to changes in pathotype (multilocus phenotypes) and infectivity frequencies. We repeatedly observed decreases in the frequency of unnecessary infectivity, suggesting that carrying multiple infectivity genes is costly for the pathogen. From an applied perspective, our results indicate that varying resistance genes in space and time can be used to help control disease, even when resistance has already been overcome. Furthermore, our approach extends our ability to test not only for the efficacy of host varieties in a given year, but also for durability over multiple cropping seasons, given variation in the combination of resistance genes deployed.

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Assessing the durability and efficiency of landscape-based strategies to deploy plant resistance to pathogens

Cited by 10 publications

References 185 publications

Careful deployment of oilseed rape crops with Rlm6 resistance gene against L. maculans is recommended to prevent the loss of efficacy of this resistance gene in French condiment mustard

Careful deployment of oilseed rape crops with Rlm6 resistance gene against L. maculans is recommended to prevent the loss of efficacy of this resistance gene in French condiment mustard

Effects of pathogen sexual reproduction on the evolutionary and epidemiological control provided by deployment strategies for two major resistance genes in agricultural landscapes

Spatio‐temporal connectivity and host resistance influence evolutionary and epidemiological dynamics of the canola pathogen Leptosphaeria maculans

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